Soluble thrombomodulin reduces inflammation and prevents microalbuminuria induced by chronic endothelial activation in transgenic mice

American Journal of Physiology - Renal Physiology

Volumn 302, Issue 6, 2012, Pages

  Rajashekhar, Gangaraju ^a   Gupta, Akanksha ^b   Marin, Abby ^a   Friedrich, Jessica ^a   Willuweit, Antje ^c   Berg, David T ^b   Cramer, Martin S ^b   Sandusky, George E ^a   Sutton, Timothy A ^a   Basile, David P ^a   Grinnell, Brian W ^b   Clauss, Matthias ^a  

^a INDIANA UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b ELI LILLY AND COMPANY   (United States)

^c MAX PLANCK INSTITUTE FOR HEART AND LUNG RESEARCH   (Germany)

Author keywords

Chronic inflammation; CKD; ICAM1; tmTNF

Indexed keywords

CD45 ANTIGEN; INTERCELLULAR ADHESION MOLECULE 1; MONOCYTE CHEMOTACTIC PROTEIN 3; RANTES; THROMBOMODULIN; TUMOR NECROSIS FACTOR ALPHA;

ALBUMINURIA; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL ACTIVATION; CELL INFILTRATION; CHEMOSENSITIVITY; CHRONIC ENDOTHELIAL CELL ACTIVATION; CHRONIC KIDNEY DISEASE; CONTROLLED STUDY; DISEASE COURSE; DOWN REGULATION; ENDOTHELIUM; ENDOTHELIUM CELL; FEMALE; GENE EXPRESSION; GENE INDUCTION; INFLAMMATION; KIDNEY FUNCTION; KIDNEY INJURY; LEUKOCYTE; MICROALBUMINURIA; MOUSE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; TRANSENDOTHELIAL AND TRANSEPITHELIAL MIGRATION; TRANSGENIC MOUSE; UPREGULATION;

EID: 84863403541     PISSN: 1931857X     EISSN: 15221466     Source Type: Journal    
DOI: 10.1152/ajprenal.00558.2011     Document Type: Article

References (51)

1. Basile DP. The endothelial cell in ischemic acute kidney injury: implications for acute and chronic function. Kidney Int 72: 151-156, 2007.
2. Basile DP, Friedrich JL, Spahic J, Knipe N, Mang H, Leonard EC, Changizi-Ashtiyani S, Bacallao RL, Molitoris BA, Sutton TA. Impaired endothelial proliferation and mesenchymal transition contribute to vascular rarefaction following acute kidney injury. Am J Physiol Renal Physiol 300: F721-F733, 2011.
3. Boehme MW, Nawroth PP, Kling E, Lin J, Amiral J, Riedesel J, Raeth U, Scherbaum WA. Serum thrombomodulin. A novel marker of disease activity in systemic lupus erythematosus. Arthritis Rheum 37: 572-577, 1994.
4. Budhiraja S, Singh J. Protein kinase C beta inhibitors: a new therapeutic target for diabetic nephropathy and vascular complications. Fundam Clin Pharmacol 22: 231-240, 2008.
5. Caramori ML, Fioretto P, Mauer M. The need for early predictors of diabetic nephropathy risk: is albumin excretion rate sufficient? Diabetes 49: 1399-1408, 2000.
6. Clauss M, Ryan J, Stern D. Modulation of endothelial cell hemostatic properties by TNF: insights into the role of endothelium in the host response to inflammatory stimuli. In: Tumor Necrosis Factors, edited by Beutler B. New York: Raven, 1992, p. 49-63.
7. Clauss M, Sunderkotter C, Sveinbjornsson B, Hippenstiel S, Willuweit A, Marino M, Haas E, Seljelid R, Scheurich P, Suttorp N, Grell M, Risau W. A permissive role for tumor necrosis factor in vascular endothelial growth factor-induced vascular permeability. Blood 97: 1321-1329, 2001.
8. Conway EM, Van de Wouwer M, Pollefeyt S, Jurk K, Van Aken H, De Vriese A, Weitz JI, Weiler H, Hellings PW, Schaeffer P, Herbert JM, Collen D, Theilmeier G. The lectin-like domain of thrombomodulin confers protection from neutrophil-mediated tissue damage by suppressing adhesion molecule expression via nuclear factor kappaB and mitogenactivated protein kinase pathways. J Exp Med 196: 565-577, 2002.
9. David S, Haller H, Kumpers P. The angiopoietin/Tie-2 axis: a novel player in chronic kidney disease. Minerva Urol Nefrol 62: 319-326, 2010.
10. David S, Kumpers P, Lukasz A, Fliser D, Martens-Lobenhoffer J, Bode-Boger SM, Kliem V, Haller H, Kielstein JT. Circulating angiopoietin-2 levels increase with progress of chronic kidney disease. Nephrol Dial Transplant 25: 2571-2576, 2010.
11. De Cock HE, Kyles AE, Griffey SM, Bernsteen L, Gregory CR. Histopathologic findings and classification of feline renal transplants. Vet Pathol 41: 244-256, 2004.
12. Elmarakby AA, Sullivan JC. Relationship between oxidative stress and inflammatory cytokines in diabetic nephropathy. Cardiovasc Ther [Epub before print].
13. Fiedler U, Reiss Y, Scharpfenecker M, Grunow V, Koidl S, Thurston G, Gale NW, Witzenrath M, Rosseau S, Suttorp N, Sobke A, Herrmann M, Preissner KT, Vajkoczy P, Augustin HG. Angiopoietin-2 sensitizes endothelial cells to TNF-alpha and has a crucial role in the induction of inflammation. Nat Med 12: 235-239, 2006.
14. Fornoni A, Ijaz A, Tejada T, Lenz O. Role of inflammation in diabetic nephropathy. Curr Diabetes Rev 4: 10-17, 2008.
15. Gurley SB, Mach CL, Stegbauer J, Yang J, Snow KP, Hu A, Meyer TW, Coffman TM. Influence of genetic background on albuminuria and kidney injury in Ins2(_/C96Y) (Akita) mice. Am J Physiol Renal Physiol 298: F788-F795, 2010.
16. He CJ, Kanfer A. Quantification and modulation of thrombomodulin activity in isolated rat and human glomeruli. Kidney Int 41: 1170-1174, 1992.
17. Ikeguchi H, Maruyama S, Morita Y, Fujita Y, Kato T, Natori Y, Akatsu H, Campbell W, Okada N, Okada H, Yuzawa Y, Matsuo S. Effects of human soluble thrombomodulin on experimental glomerulonephritis. Kidney Int 61: 490-501, 2002.
18. Isermann B, Vinnikov IA, Madhusudhan T, Herzog S, Kashif M, Blautzik J, Corat MA, Zeier M, Blessing E, Oh J, Gerlitz B, Berg DT, Grinnell BW, Chavakis T, Esmon CT, Weiler H, Bierhaus A, Nawroth PP. Activated protein C protects against diabetic nephropathy by inhibiting endothelial and podocyte apoptosis. Nat Med 13: 1349-1358, 2007.
19. Jung YJ, Kim DH, Lee AS, Lee S, Kang KP, Lee SY, Jang KY, Sung MJ, Park SK, Kim W. Peritubular capillary preservation with COMPangiopoietin-1 decreases ischemia-reperfusion-induced acute kidney injury. Am J Physiol Renal Physiol 297: F952-F960, 2009.
20. Kalaitzidis R, Bakris G. Pathogenesis and treatment of microalbuminuria in patients with diabetes: the road ahead. J Clin Hypertens (Greenwich) 11: 636-643, 2009.
21. Kaysen GA, Eiserich JP. The role of oxidative stress-altered lipoprotein structure and function and microinflammation on cardiovascular risk in patients with minor renal dysfunction. J Am Soc Nephrol 15: 538-548, 2004.
22. Kim DH, Jung YJ, Lee AS, Lee S, Kang KP, Lee TH, Lee SY, Jang KY, Moon WS, Choi KS, Yoon KH, Sung MJ, Park SK, Kim W. COMP-angiopoietin-1 decreases lipopolysaccharide-induced acute kidney injury. Kidney Int 76: 1180-1191, 2009.
23. Kumpers P, Hafer C, David S, Hecker H, Lukasz A, Fliser D, Haller H, Kielstein JT, Faulhaber-Walter R. Angiopoietin-2 in patients requiring renal replacement therapy in the ICU: relation to acute kidney injury, multiple organ dysfunction syndrome and outcome. Intensive Care Med 36: 462-470, 2010.
24. Lentz SR, Tsiang M, Sadler JE. Regulation of thrombomodulin by tumor necrosis factor-_: comparison of transcriptional and posttranscriptional mechanisms. Blood 77: 542-550, 1991.
25. Matschurat S, Blum S, Mitnacht-Kraus R, Dijkman HB, Kanal L, De Waal RM, Clauss M. Negative regulatory role of PI3-kinase in TNFinduced tumor necrosis. Int J Cancer 107: 30-37, 2003.
26. Miravete M, Klein J, Besse-Patin A, Gonzalez J, Pecher C, Bascands JL, Mercier-Bonin M, Schanstra JP, Buffin-Meyer B. Renal tubular fluid shear stress promotes endothelial cell activation. Biochem Biophys Res Commun 407: 813-817, 2011.
27. Montero A, Munger KA, Khan RZ, Valdivielso JM, Morrow JD, Guasch A, Ziyadeh FN, Badr KF. F2-isoprostanes mediate high glucoseinduced TGF-beta synthesis and glomerular proteinuria in experimental type I diabetes. Kidney Int 58: 1963-1972, 2000.
28. Ohdama S, Takano S, Ohashi K, Miyake S, Aoki N. Pentoxifylline prevents tumor necrosis factor-induced suppression of endothelial-cell surface thrombomodulin. Thromb Res 62: 745-755, 1991.
29. Ozaki T, Anas C, Maruyama S, Yamamoto T, Yasuda K, Morita Y, Ito Y, Gotoh M, Yuzawa Y, Matsuo S. Intrarenal administration of recombinant human soluble thrombomodulin ameliorates ischaemic acute renal failure. Nephrol Dial Transplant 23: 110-119, 2008.
30. Patterson CE, Clauss MA. Signaling of prolonged activation. In: Perspectives on Lung Endothelial Barrier Function, edited by Patterson CE. Amsterdam: Elsevier, 2004.
31. Prieto J, Takei F, Gendelman R, Christenson B, Biberfeld P, Patarroyo M. MALA-2, mouse homologue of human adhesion molecule ICAM-1 (CD54). Eur J Immunol 19: 1551-1557, 1989.
32. Puri TS, Shakaib MI, Chang A, Mathew L, Olayinka O, Minto AW, Sarav M, Hack BK, Quigg RJ. Chronic kidney disease induced in mice by reversible unilateral ureteral obstruction is dependent on genetic background. Am J Physiol Renal Physiol 298: F1024-F1032, 2010.
33. Rabelo LA, Alenina N, Bader M. ACE2-angiotensin-(1-7)-Mas axis and oxidative stress in cardiovascular disease. Hypertens Res 34: 154-160, 2011.
34. Rajashekhar G, Grow M, Willuweit A, Patterson CE, Clauss M. Divergent and convergent effects on gene expression and function in acute versus chronic endothelial activation. Physiol Genomics 31: 104-113, 2007.
35. Rajashekhar G, Kamocka M, Marin A, Suckow MA, Wolter WR, Badve S, Sanjeevaiah AR, Pumiglia K, Rosen E, Clauss M. Proinflammatory angiogenesis is mediated by p38 MAP kinase. J Cell Physiol 226: 800-808, 2011.
36. Rajashekhar G, Loganath A, Roy AC, Wong YC. Expression and localization of angiogenin in placenta: enhanced levels at term over first trimester villi. Mol Reprod Dev 62: 159-166, 2002.
37. Rajashekhar G, Willuweit A, Patterson CE, Sun P, Hilbig A, Breier G, Helisch A, Clauss M. Continuous endothelial cell activation increases angiogenesis: evidence for the direct role of endothelium linking angiogenesis and inflammation. J Vasc Res 43: 193-204, 2006.
38. Reiss Y, Hoch G, Deutsch U, Engelhardt B. T cell interaction with ICAM-1-deficient endothelium in vitro: essential role for ICAM-1 and ICAM-2 in transendothelial migration of T cells. Eur J Immunol 28: 3086-3099, 1998.
39. Rohnelt RK, Hoch G, Reiss Y, Engelhardt B. Immunosurveillance modelled in vitro: naive and memory T cells spontaneously migrate across unstimulated microvascular endothelium. Int Immunol 9: 435-450, 1997.
40. Romero MJ, Platt DH, Caldwell RB, Caldwell RW. Therapeutic use of citrulline in cardiovascular disease. Cardiovasc Drug Rev 24: 275-290, 2006.
41. Sharfuddin AA, Sandoval RM, Berg DT, McDougal GE, Campos SB, Phillips CL, Jones BE, Gupta A, Grinnell BW, Molitoris BA. Soluble thrombomodulin protects ischemic kidneys. J Am Soc Nephrol 20: 524-534, 2009.
42. Sironi L, Nobili E, Gianella A, Gelosa P, Tremoli E. Anti-inflammatory properties of drugs acting on the renin-angiotensin system. Drugs Today (Barc) 41: 609-622, 2005.
43. Springer TA. Traffic signals for lymphocyte recirculation and leukocyte emigration: the multistep paradigm. Cell 76: 301-314, 1994.
44. Steffen BJ, Breier G, Butcher EC, Schulz M, Engelhardt B. ICAM-1, VCAM-1, and MAdCAM-1 are expressed on choroid plexus epithelium but not endothelium and mediate binding of lymphocytes in vitro. Am J Pathol 148: 1819-1838, 1996.
45. Tsuchida A, Salem H, Thomson N, Hancock WW. Tumor necrosis factor production during human renal allograft rejection is associated with depression of plasma protein C and free protein S levels and decreased intragraft thrombomodulin expression. J Exp Med 175: 81-90, 1992.
46. Vielhauer V, Kulkarni O, Reichel CA, Anders HJ. Targeting the recruitment of monocytes and macrophages in renal disease. Semin Nephrol 30: 318-333, 2010.
47. Weiler H. Mouse models of thrombosis: thrombomodulin. Thromb Haemost 92: 467-477, 2004.
48. Willuweit A, Sass G, Schoneberg A, Eisel U, Tiegs G, Clauss M. Chronic inflammation and protection from acute hepatitis in transgenic mice expressing TNF in endothelial cells. J Immunol 167: 3944-3952, 2001.
49. Yang G, Lucas R, Caldwell R, Yao L, Romero MJ, Caldwell RW. Novel mechanisms of endothelial dysfunction in diabetes. J Cardiovasc Dis Res 1: 59-63, 2010.
50. Yang YB, Chen ZJ, Liu F, Huang SM. [The expression and significance of the angiopoietin-1 in the kidney of diabetic rats]. Sichuan Da Xue Xue Bao Yi Xue Ban 38: 93-96, 104, 2007.
51. Zhou L, Cryan EV, Minor LK, Gunnet JW, Demarest KT. A branched DNA signal amplification assay to quantitate messenger RNA of human uncoupling proteins 1, 2, and 3. Anal Biochem 282: 46-53, 2000.